Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Translational Neuroscience

Editor-in-Chief: David, Olivier

1 Issue per year

IMPACT FACTOR 2017: 0.833
5-year IMPACT FACTOR: 1.247

CiteScore 2017: 1.00

SCImago Journal Rank (SJR) 2017: 0.428
Source Normalized Impact per Paper (SNIP) 2017: 0.244

Open Access
See all formats and pricing
More options …

Similarities between cortical “up” states during slow wave sleep and wakefulness: the implications for schizophrenia

Zoran Vukadinovic
  • Department of Psychiatry and Behavioral Sciences, Montefiore Medical Center Albert Einstein College of Medicine, 111 E 210th Street, Bronx, NY, 10467, USA
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2012-03-14 | DOI: https://doi.org/10.2478/s13380-012-0004-2


Negative and positive symptoms are defining features of schizophrenia. This illness is commonly associated with a number of cognitive and affective deficits as well as with some more specific sleep abnormalities. It has been previously proposed that psychosis and positive symptoms in schizophrenia could be understood as disorders of internal brain dynamics. This proposed disordered network interplay might be particularly displayed during sleep when modulation by the senses is at the minimum. It is argued here that sleep abnormalities in schizophrenia inform our understanding of the pathomechanisms involved in psychosis. More specifically, sleep spindle initiation in NREM sleep and the preparation of sensory pathways for upcoming motor actions during wakefulness may share a common mechanism, and this shared mechanism is suggested to be impaired in schizophrenia.

Keywords: Schizophrenia; Thalamus; Psychosis; Spindles; Rebound burst firing

  • [1] Vukadinovic Z., Sleep abnormalities in schizophrenia may suggest impaired trans-thalamic cortico-cortical communication: towards a dynamic model of the illness, Eur. J. Neurosci., 2011, 34, 1031–1039 http://dx.doi.org/10.1111/j.1460-9568.2011.07822.xCrossrefWeb of ScienceGoogle Scholar

  • [2] Feinberg I., Corollary discharge, hallucinations and dreaming, Schizophr. Bull., 2011, 37, 1–3 http://dx.doi.org/10.1093/schbul/sbq115Web of ScienceCrossrefGoogle Scholar

  • [3] Destexhe A., Intracellular and computational evidence for a dominant role of internal network activity in cortical computations, Curr. Opin. Neurobiol., 2011, 21, 717–725 http://dx.doi.org/10.1016/j.conb.2011.06.002CrossrefWeb of ScienceGoogle Scholar

  • [4] Vukadinovic Z., Rosenzweig I., Abnormalities in thalamic neurophysiology in schizophrenia: could psychosis be a result of potassium channel dysfunction?, Neurosci. Biobehav. Rev., 2012, 36, 960–968 http://dx.doi.org/10.1016/j.neubiorev.2011.11.005CrossrefGoogle Scholar

  • [5] Destexhe A., Hughes S. W., Rudolph M., Crunelli V., Are corticothalamic UP states fragments of wakefulness? Trends Neurosci., 2007, 30, 334–342 http://dx.doi.org/10.1016/j.tins.2007.04.006CrossrefWeb of ScienceGoogle Scholar

  • [6] Huffaker S. J., Chan J., Nicodemus K. K., Sambataro F., Yang F., Mattay V., et al., Primate-specific, brain isoform of KCNH2 affects cortical physiology, cognition, neuronal repolarization and risk of schizophrenia, Nat. Med., 2009, 15, 509–518 http://dx.doi.org/10.1038/nm.1962Web of ScienceCrossrefGoogle Scholar

  • [7] Mölle M., Marshall L., Gais S., Born J., Grouping of spindle activity during slow oscillations in human non-rapid eye movement sleep, J. Neurosci., 2002, 22, 10941–10947 Google Scholar

  • [8] Steriade M., Neuronal substrates of sleep and epilepsy, Cambridge University Press, Cambridge, UK, 2003 Google Scholar

  • [9] Bazhenov M., Timofeev I., Steriade M., Sejnowski T., Spiking-bursting activity in the thalamic reticular nucleus initiates sequences of spindle oscillations in thalamic networks, J. Neurophysiol., 2000, 84, 1076–1087 Google Scholar

  • [10] Sherman S. M., Guillery R. W., Exploring the thalamus and its role in cortical function, 2nd ed., The MIT Press, Cambridge, USA, 2006 Google Scholar

  • [11] Kim U., Sanchez-Vives M. V., McCormick D. A., Functional dynamics of GABAergic inhibition in the thalamus, Science, 1997, 278, 130–134 http://dx.doi.org/10.1126/science.278.5335.130CrossrefGoogle Scholar

  • [12] Steriade M., Grouping of brain rhythms in corticothalamic systems, Neuroscience, 2006, 137, 1087–1106 http://dx.doi.org/10.1016/j.neuroscience.2005.10.029CrossrefGoogle Scholar

  • [13] Sherman S. M., Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci., 2001, 24, 122–126 http://dx.doi.org/10.1016/S0166-2236(00)01714-8CrossrefGoogle Scholar

  • [14] Fuentealba P., Timofeev I., Steriade M., Prolonged hyperpolarizing potentials precede spindle oscillations in the thalamic reticular nucleus, Proc. Natl. Acad. Sci. USA, 2004, 101, 9816–9821 http://dx.doi.org/10.1073/pnas.0402761101CrossrefGoogle Scholar

  • [15] Neto F. L., Schadrack J., Berthele A., Zieglgänsberger W., Tölle T. R., Castro-Lopez J. M., Differential distribution of metabotropic glutamate receptors subty pe mRNAs in the thalamus of the rat, Brain Res., 2000, 854, 93–105 http://dx.doi.org/10.1016/S0006-8993(99)02326-4CrossrefGoogle Scholar

  • [16] Ohishi H., Shigemoto R., Nakanishi S., Mizuno N., Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an in situ hybridization study, J. Comp. Neurol., 1993, 335, 252–266 http://dx.doi.org/10.1002/cne.903350209CrossrefGoogle Scholar

  • [17] Coutinho V., Knöpfel T., Book review: metabotropic glutamate receptors: electrical and chemical signaling properties, Neuroscientist, 2002, 8, 551–561 http://dx.doi.org/10.1177/1073858402238514CrossrefGoogle Scholar

  • [18] Cox C. L., Sherman S. M., Glutamate inhibits thalamic reticular neurons, J. Neurosci., 1999, 19, 6694–6699 Google Scholar

  • [19] Alexander G. M., Godwin D. W., Unique presynaptic and postsynaptic roles of group II metabotropic glutamate receptors in the modulation of thalamic network activity, Neurosci., 2006, 141, 501–513 http://dx.doi.org/10.1016/j.neuroscience.2006.03.060CrossrefGoogle Scholar

  • [20] Govindaiah G., Cox C. L., Metabotropic glutamate receptors differentially regulate GABAergic inhibition in thalamus, J. Neurosci., 2006, 26, 13443–13453 http://dx.doi.org/10.1523/JNEUROSCI.3578-06.2006CrossrefGoogle Scholar

  • [21] Turner J. P., Salt T. E., Group II and III metabotropic glutamate receptors and the control of nucleus reticularis thalami input to rat thalamocortical neurones in vitro, Neuroscience, 2003, 122, 459–469 http://dx.doi.org/10.1016/j.neuroscience.2003.08.014CrossrefGoogle Scholar

  • [22] Ferrarelli F., Huber R., Peterson M. J., Massimini M., Murphy M., Riedner B. A. et al., Reduced sleep spindle activity in schizophrenia patients, Am. J. Psychiatry, 2007, 164, 483–492 http://dx.doi.org/10.1176/appi.ajp.164.3.483CrossrefGoogle Scholar

  • [23] Ferrarelli F., Peterson M. J., Sarasso S., Riedner B. A., Murphy M. J., Benca R. M., et al., Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles, Am. J. Psychiatry, 2010, 167, 1339–1348 http://dx.doi.org/10.1176/appi.ajp.2010.09121731CrossrefGoogle Scholar

  • [24] Manoach D. S., Thakkar K. N., Stroynowski E., Ely A., McKinley S. K., Wamsley E. et al., Reduced overnight consolidation of procedural learning in chronic medicated schizophrenia is related to specific sleep stages, J. Psychiatr. Res., 2010, 44, 112–120 http://dx.doi.org/10.1016/j.jpsychires.2009.06.011CrossrefWeb of ScienceGoogle Scholar

  • [25] Seeck-Hirschner M., Baier P. C., Sever S., Buschbacher A., Aldenhoff J. B., Göder R., Effects of daytime naps on procedural and declarative memory in patients with schizophrenia, J. Psychiatr. Res., 2009, 44, 42–47 http://dx.doi.org/10.1016/j.jpsychires.2009.05.008Web of ScienceCrossrefGoogle Scholar

  • [26] Wamsley E. J., Tucker M. A., Schinn A. K., Ono K. E., McKinley S. K., Ely A. V. et al., Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation?, Biol. Psychiatry, 2012, 71, 154–161 http://dx.doi.org/10.1016/j.biopsych.2011.08.008Web of ScienceCrossrefGoogle Scholar

  • [27] Hiatt J. F., Floyd T. C., Katz P. H., Feinberg I., Further evidence of abnormal non-rapid-eye movement sleep in schizophrenia, Arch. Gen. Psychiatry, 1985, 42, 797–802 http://dx.doi.org/10.1001/archpsyc.1985.01790310059007CrossrefGoogle Scholar

  • [28] Poulin J., Daoust A. M., Forest G., Stip E., Godbout R., Sleep architecture and its clinical correlates in first episode and neuroleptic-naïve patients with schizophrenia, Schizophr. Res., 2003, 62, 147–153 http://dx.doi.org/10.1016/S0920-9964(02)00346-8CrossrefGoogle Scholar

  • [29] Van Cauter E., Linkowski P., Kerkhofs M., Hubain P., L’Hermite-Baleriaux M., Leclercq R. et al., Circadian and sleep-related endocrine rhythms in schizophrenia, Arch. Gen. Psychiatry, 1991, 48, 348–356 http://dx.doi.org/10.1001/archpsyc.1991.01810280064009CrossrefGoogle Scholar

  • [30] Shepard P. D., Canavier C. C., Levitan E. S., Ether-a-go-go-related gene potassium channels: what’s all the buzz about?, Schizophr. Bull., 2007, 33, 1263–1269 http://dx.doi.org/10.1093/schbul/sbm106Web of ScienceCrossrefGoogle Scholar

  • [31] Papa M., Boscea F., Canitano A., Castaldo P., Selletti S., Annunziato L. et al., Expression pattern of the ether-a-gogo-related (ERG) K+ channel-encoding genes ERG1, ERG2, and ERG3 in the adult rat central nervous system, J. Comp. Neurol., 2003, 466, 119–135 http://dx.doi.org/10.1002/cne.10886Google Scholar

  • [32] Saganich M. J., Machado E., Rudy B., Differential expression of genes encoding subthreshold-operating voltage-gated K+ channels in brain, J. Neurosci., 2001, 21, 4609–4624 Google Scholar

  • [33] Moghaddam B., Adams B. W., Reversal of phencyclidine effects by a group II metabotropic glutamate receptor agonist in rats, Science, 1998, 281, 1349–1352 http://dx.doi.org/10.1126/science.281.5381.1349CrossrefGoogle Scholar

  • [34] Patil, S. T., Zhang L., Martenyi F., Lowe S. L., Jackson K. A., Andreev B. V. et al., Activation of mGlu2/3 receptors as a new approach to treat schizophrenia: a randomized phase 2 clinical trial, Nat. Med., 2007, 13, 1102–1107 http://dx.doi.org/10.1038/nm1632CrossrefWeb of ScienceGoogle Scholar

  • [35] Olszewski R. T., Bukhari N., Zhou J., Kozikowski A. P., Wroblewski J. T., Shamimi-Noori S. et al., NAAG peptidase inhibition reduces locomotor activity and some stereotypes in the PCP model of schizophrenia via group II mGluR, J. Neurochem., 2004, 89, 876–885 http://dx.doi.org/10.1111/j.1471-4159.2004.02358.xCrossrefGoogle Scholar

  • [36] Ribeiro T. L., Copelli M., Caixeta F., Belchior H., Chialvo D. R., Nicolelis M. A. L. et al., Spike avalanches exhibit universal dynamics across the sleep-wake cycle, PLoS One, 2010, 5, e14129 http://dx.doi.org/10.1371/journal.pone.0014129CrossrefGoogle Scholar

  • [37] Marsat G., Pollack G. S., A behavioral role for feature detection by sensory bursts, J. Neurosci., 2006, 26, 10542–10547 http://dx.doi.org/10.1523/JNEUROSCI.2221-06.2006CrossrefGoogle Scholar

  • [38] Destexhe A., Sejnowski T. J., The initiation of bursts in thalamic neurons and the cortical control of thalamic sensitivity, 2002, Phil. Trans. R. Soc. Lond. B, 357, 1649–1657 http://dx.doi.org/10.1098/rstb.2002.1154CrossrefGoogle Scholar

  • [39] Fuster J. M., The prefrontal cortex, 4th ed., Elsevier, London, UK, 2008 Google Scholar

  • [40] Rosenzweig I, Varga ET, Akeson P, Beniczky S., Simple autonomic seizures and ictal enuresis, Seizure. 2011, 20, 662–664. http://dx.doi.org/10.1016/j.seizure.2011.04.009Web of ScienceCrossrefGoogle Scholar

  • [41] Zikopoulos B., Barbas H., Circuits for multisensory integration and attentional modulation through the prefrontal cortex and the thalamic reticular nucleus in primates, Rev. Neurosci., 2007, 18, 417–438 http://dx.doi.org/10.1515/REVNEURO.2007.18.6.417CrossrefGoogle Scholar

  • [42] Frith C.D., Blackemore S.J., Wolpert D.M., Explaining the symptoms of schizophrenia: Abnormalities in the awareness of action, Brain. Res. Rev., 2000, 31, 357–363 http://dx.doi.org/10.1016/S0165-0173(99)00052-1CrossrefGoogle Scholar

  • [43] Lisman J.E., Hyun J.P., Zhang Y., Otmakhova N.A., A thalamohippocampal-ventral tegmental area loop may produce the positive feedback that underlies the psychotic break in schizophrenia, Biol. Psychiatry, 2010, 68, 17–24 http://dx.doi.org/10.1016/j.biopsych.2010.04.007CrossrefWeb of ScienceGoogle Scholar

  • [44] Govindaiah G., Wang Y., Cox C.L., Dopamine enhances the excitability of somatosensory thalamocortical neurons, Neuroscience, 2010, 170(4), 981–991 http://dx.doi.org/10.1016/j.neuroscience.2010.08.043Web of ScienceCrossrefGoogle Scholar

  • [45] Buzsaki G., Petit mal epilepsy and parkinsonian tremor: hypothesis of a common pacemaker, Neuroscience, 1990, 36(1), 1–14 http://dx.doi.org/10.1016/0306-4522(90)90345-5CrossrefGoogle Scholar

  • [46] Buzsaki G., The thalamic clock: emergent network properties, Neuroscience, 1991, 41(2/3), 351–364 http://dx.doi.org/10.1016/0306-4522(91)90332-ICrossrefGoogle Scholar

  • [47] Moghaddam B., Dopamine in the thalamus: a hotbed for psychosis?, Biol. Psychiatry, 2010, 68, 3–4 http://dx.doi.org/10.1016/j.biopsych.2010.05.014CrossrefWeb of ScienceGoogle Scholar

  • [48] Lüscher C., Slesinger P.A., Emerging roles for G protein-gated inwardly rectifying potassium (GIRK) channels in health and disease, Nat. Rev. Neurosci., 2010, 11, 301–315 http://dx.doi.org/10.1038/nrn2834Web of ScienceCrossrefGoogle Scholar

About the article

Published Online: 2012-03-14

Published in Print: 2012-03-01

Citation Information: Translational Neuroscience, Volume 3, Issue 1, Pages 51–55, ISSN (Online) 2081-6936, ISSN (Print) 2081-3856, DOI: https://doi.org/10.2478/s13380-012-0004-2.

Export Citation

© 2012 Versita Warsaw. This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License. BY-NC-ND 3.0

Citing Articles

Here you can find all Crossref-listed publications in which this article is cited. If you would like to receive automatic email messages as soon as this article is cited in other publications, simply activate the “Citation Alert” on the top of this page.

Zoran Vukadinovic
Translational Neuroscience, 2012, Volume 3, Number 4

Comments (0)

Please log in or register to comment.
Log in